Persistent persister misperceptions

Frontiers in Microbiology

Volumn 7, Issue DEC, 2016, Pages

  Kim, Jun Seob ^a   Wood, Thomas K ^a  

^a The Pennsylvania State University   (United States)

Author keywords

Antimicrobial tolerance; Persister cells

Indexed keywords

AMINOGLYCOSIDE ANTIBIOTIC AGENT; ANTIBIOTIC AGENT; BORIC ACID; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CHLORAMPHENICOL; CIPROFLOXACIN; CYCLIC AMP; ENDOPEPTIDASE LA; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; INDOLE; INDOLE DERIVATIVE; ISONIAZID; OFLOXACIN; PENICILLIN BINDING PROTEIN; PENICILLIN DERIVATIVE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN; TOLC PROTEIN; TRANSCRIPTOME;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; BACTERIAL INFECTION; BACTERIAL STRAIN; BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING THE ENTIRE ORGANISM; CELL KILLING; CELL SURVIVAL; CELLS BY FUNCTION; ESCHERICHIA COLI; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC VARIABILITY; NONHUMAN; PATHOGENICITY; PERSISTER CELL; PHENOTYPE; PSEUDOMONAS AERUGINOSA; SHORT SURVEY; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TRANSCRIPTOMICS;

EID: 85009413812     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.02134     Document Type: Short Survey

References (62)

1. Allison, K. R., Brynildsen, M. P., and Collins, J. J. (2011). Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 473, 216-220. doi: 10.1038/nature10069
2. Amato, S. M., Orman, M. A., and Brynildsen, M. P. (2013). Metabolic control of persister formation in Escherichia coli. Mol. Cell 50, 475-487. doi: 10.1016/j.molcel.2013.04.002
3. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L., and Leibler, S. (2004). Bacterial persistence as a phenotypic switch. Science 305, 1622-1625. doi: 10.1126/science.1099390
4. Bansal, T., Alaniz, R. C., Wood, T. K., and Jayaraman, A. (2010). The bacterial signal indole promotes epithelial cell barrier properties and attenuates inflammation. Proc. Natl. Acad. Sci. U.S.A. 107, 228-233. doi: 10.1073/pnas.0906112107
5. Bigger, J. W. (1944). Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244, 497-500. doi: 10.1016/S0140-6736(00)74210-3
6. Brauner, A., Fridman, O., Gefen, O., and Balaban, N. Q. (2016). Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat. Rev. Microbiol. 14, 320-330. doi: 10.1038/nrmicro.2016.34
7. Chowdhury, N., Kwan, B. W., and Wood, T. K. (2016a). Persistence increases in the absence of the alarmone guanosine tetraphosphate by reducing cell growth. Sci. Rep. 6, 20519. doi: 10.1038/srep20519
8. Chowdhury, N., Wood, T. L., Martínez-Vázquez, M., García-Contreras, R., and Wood, T. K. (2016b). DNA-crosslinker cisplatin eradicates bacterial persister cells. Biotechnol. Bioeng. 113, 1984-1992. doi: 10.1002/bit.25963
9. Chu, W., Zere, T. R., Weber, M. M., Wood, T. K., Whiteley, M., Hidalgo-Romano, B., et al. (2012). Indole production promotes Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling. Appl. Environ. Microbiol. 78, 411-419. doi: 10.1128/aem.06396-11
10. Conlon, B. P., Rowe, S. E., Gandt, A. B., Nuxoll, A. S., Donegan, N. P., Zalis, E. A., et al. (2016). Persister formation in Staphylococcus aureus is associated with ATP depletion. Nat. Microbiol. 1:16051. doi: 10.1038/nmicrobiol.2016.51
11. Cruz-Muñiz, M. Y., López-Jacome, L. E., Hernández-Durán, M., Franco-Cendejas, R., Licona-Limón, P., Ramos-Balderas, J. L., et al. (2016). Repurposing the anticancer drug mitomycin C for the treatment of persistent Acinetobacter baumannii infections. Int. J. Antimicrob doi: 10.1016/j.ijantimicag.2016.08.022 [Epub ahead of print]
12. Dörr, T., Vulic, M., and Lewis, K. (2010). Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol. 8:e1000317. doi: 10.1371/journal.pbio.1000317
13. Fauvart, M., De Groote, V. N., and Michiels, J. (2011). Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J. Med. Microbiol. 60, 699-709. doi: 10.1099/jmm.0.030932-0
14. Germain, E., Roghanian, M., Gerdes, K., and Maisonneuve, E. (2015). Stochastic induction of persister cells by HipA through (p)ppGpp-mediated activation of mRNA endonucleases. Proc. Natl. Acad. Sci. U.S.A. 112, 5171-5176. doi: 10.1073/pnas.1423536112
15. Guo, Y., Quiroga, C., Chen, Q., McAnulty, M. J., Benedik, M. J., Wood, T. K., et al. (2014). RalR (a DNase) and RalA (a small RNA) form a type I toxin-antitoxin system in Escherichia coli. Nucleic Acids Res. 42, 6448-6462. doi: 10.1093/nar/gku279
16. Hansen, S., Lewis, K., and Vulic, M. (2008). Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob. Agents Chemother. 52, 2718-2726. doi: 10.1128/aac.00144-08
17. Harrison, J. J., Wade, W. D., Akierman, S., Vacchi-Suzzi, C., Stremick, C. A., Turner, R. J., et al. (2009). The chromosomal toxin gene yafQ is a determinant of multidrug tolerance for Escherichia coli growing in a biofilm. Antimicrob. Agents Chemother. 53, 2253-2258. doi: 10.1128/aac.00043-09
18. Henry, T. C., and Brynildsen, M. P. (2016). Development of Persister-FACSeq: a method to massively parallelize quantification of persister physiology and its heterogeneity. Sci. Rep. 6:25100. doi: 10.1038/srep25100
19. Hidalgo-Romano, B., Gollihar, J., Brown, S. A., Whiteley, M., Valenzuela, E., Kaplan, H. B., et al. (2014). Indole inhibition of N-acylated homoserine lactone-mediated quorum signalling is widespread in Gram-negative bacteria. Microbiology 160, 2464-2473. doi: 10.1099/mic.0.081729-0
20. Hirakawa, H., Inazumi, Y., Masaki, T., Hirata, T., and Yamaguchi, A. (2005). Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol. Microbiol. 55, 1113-1126. doi: 10.1111/j.1365-2958.2004.04449.x
21. Hobby, G. L., Meyer, K., and Chaffee, E. (1942). Observations on the mechanism of action of penicillin. Exp. Biol. Med. 50, 281-285. doi: 10.3181/00379727-50-13773
22. Hong, S. H., Wang, X., O'Connor, H. F., Benedik, M. J., and Wood, T. K. (2012). Bacterial persistence increases as environmental fitness decreases. Microb. Biotechnol. 5, 509-522. doi: 10.1111/j.1751-7915.2011.00327.x
23. Hu, Y., and Coates, A. R. M. (2005). Transposon mutagenesis identifies genes which control antimicrobial drug tolerance in stationary-phase Escherichia coli. FEMS Microbiol. Lett. 243, 117-124. doi: 10.1016/j.femsle.2004.11.049
24. Hu, Y., Kwan, B. W., Osbourne, D. O., Benedik, M. J., and Wood, T. K. (2015). Toxin YafQ increases persister cell formation by reducing indole signalling. Environ. Microbiol. 17, 1275-1285. doi: 10.1111/1462-2920.12567
25. Kaldalu, N., Hauryliuk, V., and Tenson, T. (2016). Persisters-as elusive as ever. Appl. Microbiol. Biotechnol. 100, 6545-6553. doi: 10.1007/s00253-016-7648-8
26. Keren, I., Shah, D., Spoering, A., Kaldalu, N., and Lewis, K. (2004). Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186, 8172-8180. doi: 10.1128/JB.186.24.8172-8180.2004
27. Kim, Y., and Wood, T. K. (2010). Toxins Hha and CspD and small RNA regulator Hfq are involved in persister cell formation through MqsR in Escherichia coli. Biochem. Biophys. Res. Commun. 391, 209-213. doi: 10.1016/j.bbrc.2009.11.033
28. Kobayashi, A., Hirakawa, H., Hirata, T., Nishino, K., and Yamaguchi, A. (2006). Growth phase-dependent expression of drug exporters in Escherichia coli and its contribution to drug tolerance. J. Bacteriol. 188, 5693-5703. doi: 10.1128/JB.00217-06
29. Korch, S. B., Henderson, T. A., and Hill, T. M. (2003). Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol. Microbiol. 50, 1199-1213. doi: 10.1046/j.1365-2958.2003.03779.x
30. Kwan, B. W., Chowdhury, N., and Wood, T. K. (2015a). Combatting bacterial infections by killing persister cells with mitomycin C. Environ. Microbiol. 17, 4406-4414. doi: 10.1111/1462-2920.12873
31. Kwan, B. W., Osbourne, D. O., Hu, Y., Benedik, M. J., and Wood, T. K. (2015b). Phosphodiesterase DosP increases persistence by reducing cAMP which reduces the signal indole. Biotechnol. Bioeng. 112, 588-600. doi: 10.1002/bit.25456
32. Kwan, B. W., Valenta, J. A., Benedik, M. J., and Wood, T. K. (2013). Arrested protein synthesis increases persister-like cell formation. Antimicrob. Agents Chemother. 57, 1468-1473. doi: 10.1128/AAC.02135-12
33. Lee, J., Attila, C., Cirillo, S. L., Cirillo, J. D., and Wood, T. K. (2009). Indole and 7-hydoxyindole diminish Pseudomonas aeruginosa virulence. Microb. Biotechnol. 2, 75-90. doi: 10.1111/j.1751-7915.2008.00061.x
34. Lee, J., Bansal, T., Jayaraman, A., Bentley, W. E., and Wood, T. K. (2007a). Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl. Environ. Microbiol. 73, 4100-4109. doi: 10.1128/AEM.00360-07
35. Lee, J., Jayaraman, A., and Wood, T. K. (2007b). Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7:42. doi: 10.1186/1471-2180-7-42
36. Lee, J., Zhang, X.-S., Hegde, M., Bentley, W. E., Jayaraman, A., and Wood, T. K. (2008). Indole cell signaling occurs primarily at low temperatures in Escherichia coli. ISME J. 2, 1007-1023. doi: 10.1038/ismej.2008.54
37. Lee, J.-H., Kim, Y.-G., Gwon, G., Wood, T. K., and Lee, J. (2016). Halogenated indoles eradicate bacterial persister cells and biofilms. AMB Express 6, 123. doi: 10.1186/s13568-016-0297-6
38. Luidalepp, H., Jõers, A., Kaldalu, N., and Tenson, T. (2011). Age of inoculum strongly influences persister frequency and can mask effects of mutations implicated in altered persistence. J. Bacteriol. 193, 3598-3605. doi: 10.1128/jb.00085-11
39. Maisonneuve, E., Castro-Camargo, M., and Gerdes, K. (2013). (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154, 1140-1150. doi: 10.1016/j.cell.2013.07.048
40. Maisonneuve, E., Shakespeare, L. J., Jørgensen, M. G., and Gerdes, K. (2011). Bacterial persistence by RNA endonucleases. Proc. Natl. Acad. Sci. U.S.A. 108, 13206-13211. doi: 10.1073/pnas.1100186108
41. Möker, N., Dean, C. R., and Tao, J. (2010). Pseudomonas aeruginosa increases formation of multidrug-tolerant persister cells in response to quorum-sensing signaling molecules. J. Bacteriol. 192, 1946-1955. doi: 10.1128/jb.01231-09
42. Moyed, H. S., and Bertrand, K. P. (1983). hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 155, 768-775.
43. Orman, M. A., and Brynildsen, M. P. (2013). Dormancy is not necessary or sufficient for bacterial persistence. Antimicrob. Agents Chemother. 57, 3230-3239. doi: 10.1128/aac.00243-13
44. Osbourne, D. O., Soo, V. W. C., Konieczny, I., and Wood, T. K. (2014). Polyphosphate, cyclic AMP, guanosine tetraphosphate, and c-di-GMP reduce in vitro Lon activity. Bioengineered 5, 264-268. doi: 10.4161/bioe.29261
45. Pecota, D. C., and Wood, T. K. (1996). Exclusion of T4 Phage by the hok/sok killer locus from plasmid R1. J. Bacteriol. 178, 2044-2050. doi: 10.1128/jb.178.7.2044-2050.1996
46. Pu, Y., Zhao, Z., Li, Y., Zou, J., Ma, Q., Zhao, Y., et al. (2016). Enhanced efflux activity facilitates drug tolerance in dormant bacterial cells. Mol. Cell 62, 284-294. doi: 10.1016/j.molcel.2016.03.035
47. Ramisetty, B. C. M., Ghosh, D., Roy Chowdhury, M., and Santhosh, R. S. (2016). What is the link between stringent response, endoribonuclease encoding type ii toxin-antitoxin systems and persistence? Front. Microbiol. 7:1882. doi: 10.3389/fmicb.2016.01882
48. Rasko, D. A., and Sperandio, V. (2010). Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. Drug Discov. 9, 117-128. doi: 10.1038/nrd3013
49. Schumacher, M. A., Balani, P., Min, J., Chinnam, N. B., Hansen, S., Vulic, M., et al. (2015). HipBA-promoter structures reveal the basis of heritable multidrug tolerance. Nature 524, 59-64. doi: 10.1038/nature14662
50. Shah, D., Zhang, Z., Khodursky, A., Kaldalu, N., Kurg, K., and Lewis, K. (2006). Persisters: a distinct physiological state of E. coli. BMC Microbiol. 6:53. doi: 10.1186/1471-2180-6-53
51. Shan, Y., Lazinski, D., Rowe, S., Camilli, A., and Lewis, K. (2015). Genetic basis of persister tolerance to aminoglycosides in Escherichia coli. mBio 6, e78-15. doi: 10.1128/mBio.00078-15
52. Shimada, Y., Kinoshita, M., Harada, K., Mizutani, M., Masahata, K., Kayama, H., et al. (2013). Commensal bacteria-dependent indole production enhances epithelial barrier function in the colon. PLoS ONE 8:e80604. doi: 10.1371/journal.pone.0080604
53. Spoering, A. L., Vulic, M., and Lewis, K. (2006). GlpD and PlsB participate in persister cell formation in Escherichia coli. J. Bacteriol. 188, 5136-5144. doi: 10.1128/jb.00369-06
54. Tan, Q., Awano, N., and Inouye, M. (2011). YeeV is an Escherichia coli toxin that inhibits cell division by targeting the cytoskeleton proteins, FtsZ and MreB. Mol. Microbiol. 79, 109-118. doi: 10.1111/j.1365-2958.2010.07433.x
55. Van den Bergh, B., Michiels, J. E., Wenseleers, T., Windels, E. M., Boer, P. V., Kestemont, D., et al. (2016). Frequency of antibiotic application drives rapid evolutionary adaptation of Escherichia coli persistence. Nat. Microbiol. 1:16020. doi: 10.1038/nmicrobiol.2016.20
56. Vega, N. M., Allison, K. R., Khalil, A. S., and Collins, J. J. (2012). Signaling-mediated bacterial persister formation. Nat. Chem. Biol. 8, 431-433. doi: 10.1038/nchembio.915
57. Verstraeten, N., Knapen, W. J., Kint, C. I., Liebens, V., Van den Bergh, B., Dewachter, L., et al. (2015). Obg and membrane depolarization are part of a microbial bet-hedging strategy that leads to antibiotic tolerance. Mol. Cell 59, 9-21. doi: 10.1016/j.molcel.2015.05.011
58. Wakamoto, Y., Dhar, N., Chait, R., Schneider, K., Signorino-Gelo, F., Leibler, S., et al. (2013). Dynamic persistence of antibiotic-stressed mycobacteria. Science 339, 91-95. doi: 10.1126/science.1229858
59. Wang, X., Lord, D. M., Cheng, H.-Y., Osbourne, D. O., Hong, S. H., Sanchez-Torres, V., et al. (2012). A Novel type V TA system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat. Chem. Biol. 8, 855-861. doi: 10.1038/nchembio.1062
60. Wood, T. K. (2016). Combatting bacterial persister cells. Biotechnol. Bioeng. 113, 476-483. doi: 10.1002/bit.25721
61. Wood, T. K., Knabel, S. J., and Kwan, B. W. (2013). Bacterial persister cell formation and dormancy. Appl. Environ. Microbiol. 79, 7116-7121. doi: 10.1128/AEM.02636-13
62. Yamaguchi, Y., Park, J., and Inouye, M. (2011). Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45, 61-79. doi: 10.1146/annurev-genet-110410-132412